Structural Characteristics of Cell Walls of Kenaf (Hibiscus Cannabinus L.) and ﬁxation of Carbon Dioxide

J Wood Sci (2003) 49:255–261 © The Japan Wood Research Society 2003

ORIGINAL ARTICLE

Thi Bach Tuyet Lam · Keko Hori · Kenji Iiyama Structural characteristics of cell walls of kenaf (Hibiscus cannabinus L.) and ﬁxation of carbon dioxide

Received: April 22, 2002 / Accepted: July 24, 2002

Abstract Kenaf (Hibiscus cannabinus) plants are widely Introduction known for their contribution to the global and regional environment because of their ability to fix CO2. On the Kenaf (Hibiscus cannabinus L.) has attracted increasing other hand, some scientists have doubts about CO2 fixation by kenaf and have misgivings about the effect of kenaf on interest from the viewpoint of preserving the global envi- the ecosystem. We have characterized the structural charac- ronment because of the significantly high rate of CO2 accu- 1,2 teristics of cell walls of bast fibers, cores, roots, and leaves mulation. There have been reports on the management of 3–8 of kenaf during the maturation of plants and investigated cropping and cultivation and on the morphological char- 9–11 the rate of photosynthesis. During maturation of the kenaf acterization of fiber. It would be expected that as a raw plant the cellulose (bast fiber 52–59%, core 44–46%) and material it might be an alternative to wood fiber in the pulp 12–16 lignin (bast fiber 9.3–13.2%, core 18.3–23.2%) contents in- and paper industry to avoid destruction of forests. Fur- creased significantly. The aromatic composition of the lig- thermore, the lignin in the cell walls has been of interest for nin of bast fiber was significantly different from that of the its chemical structural features, as an unusually high ratio of 13,17–20 core lignin and of other plants. The lignin of bast fiber syringyl/guaiacyl nuclei has been reported. 21–26 appears similar to pure syringyl lignin. Fixation of CO by Products such as paper, charcoal, nonwoven matting 2 27 28–31 32 kenaf plants and their contribution to the global environ- in the automotive industry, textiles, carbon fiber, graft 33,34 35 36 ment are discussed. A significatly high rate of photosynthe- polymer, particleboard, composites with minerals, 27,37,38 39 sis of kenaf plants was observed compared to that of woody composites with synthetic polymers, potting soil, liquefaction,40 and animal bedding can all be produced from plants in Japan, but the amount of CO2 fixation depends on the characteristics of the plantation. If the kenaf was kenaf. In addition, the kenaf plant is being watched with keen interest as a source of phytoremediation.41–46 planted in high density, about twice as much CO2 was fixed as was fixed by trees in a tropical rain forest. In this paper the chemical composition of the cell walls of bast fiber, core, and roots of kenaf plants being grown in a Key words Kenaf · Hibiscus cannabinus · Lignin · Neutral greenhouse and matured kenaf plants were analyzed, and sugar · Cell wall · Rate of photosynthesis · Fixation of car- their structural features were characterized. In addition, the bon dioxide rate of photosynthesis and fixation of CO2 by the kenaf plant were examined.

Materials and methods

Plants T.B.T. Lam School of Botany, University of Melbourne, Victoria 3010, Australia Seeds of varieties Chinpi-3 and Everglades of kenaf (Hibis- K. Hori cus cannabinus) were kindly supplied by the Japan Kenaf Graduate School of Agricultural and Life Sciences, the University of Association. Both varieties were sown on 13 April 1999 in Tokyo, Tokyo 113-8657, Japan pots with commercial mixed fertilizer in a greenhouse at the K. Iiyama (*) Forestry and Forest Products Research Institute, Tsukuba, Asian Natural Environmental Science Center, the University of Japan. Then 5–10 plants were harvested at 30, 36, 43, 49, 52, Tokyo, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan Tel. ϩ81-3-5841-2783; Fax ϩ81-3-5841-5230 59, 68, 90, and 121 days. The plants were frozen im- e-mail: [email protected]. mediately after harvesting and then freeze-dried. The dried 256 plants were separated into bast fibers, stem cores, leaves, Isolation and characterization of native (Björkman) lignin and roots. The weight of each tissue was determined after further drying in a vacuum oven for 48h at 40°C. Kenaf Extract-free samples of bast fibers, cores, and leaves of fibers for rope production from matured plants (variety Chinpi-3 variety grown for 121 days were finely ground VN-1, harvested in Vietnam) and fiber and core for paper- with a vibration ball mill for 72h with no solvent;53 they making (variety Chinpi-3, harvested in China) were gifts of were cooled by water flow. Lignin was isolated with the Thai Binh Jute Co. Vietnam and Japanese Association of Björkman procedure54 and then characterized by acetyl Non-Wood Paper Promotion, respectively. Dried tissue was determination.51 13C-NMR spectra of the lignin were mea- µ 1 milled with a Wiley mill to pass 420 m sieves, extracted sured in (CD3)2SO; and the H-NMR spectra in CDCl3 with boiling 80% aqueous EtOH (1h, ϫ3), followed with were investigated after acetylation with acetic anhydride- hot water overnight at 65°C. pyridine.

Chemical composition Rate of photosynthesis and biomass production

The lignin content of the extract-free sample was analyzed The rate of photosynthesis of kenaf leaves in the green- by an acetyl bromide procedure.47 The neutral sugar and house and some leaves of other outdoor plants were uronic acids composition in the hydrolysate after H2SO4 determined at 31, 38, and 28 days, using the Shimadzu hydrolysis of the sample was determined by alditol-acetate48 potable photosynthesis-evaporation analyzer SPB-H3. The and colorimetric49 procedures, respectively. Cellulose rate was corrected for a photon density of 1000µmol/cm2/s. content was estimated as the content of anhydroglucosyl Kenaf (H. cannabinus L. var. VN-1) was cultivated under residue. Hydroxycinnamic acids that were ester- and various cultivation densities (222000–555000 plants/ha) at ether-linked to cell wall polymers were quantiﬁed by the Thu Duc District, Ho Chi Minh City by Dr. Quang Hung procedure of Lam and coworkers.50 The acetyl content was Le, College of Agriculture and Forestry, Ho Chi Minh City, determined by an 1H-nuclear magnetic resonance (NMR) Vietnam. procedure after hydrolysis with 25% (v/v) D2SO4/D2O using EtOH as an internal standard.51 The aromatic composition of lignin was investigated by an alkaline nitrobenzene oxi- Results and discussion dation procedure.52 The sample was combusted for 3h at 700°C to quantify the total ash content. The ash was dis- solved in 0.5M HCl with heating, and calcium and magne- Chemical composition sium were quantiﬁed using atomic absorption spectroscopy (Hitachi Z-6100). The chemical compositions of matured kenaf samples supplied from Vietnam and China are shown in Table 1 and compared with those of typical temperate woody species: spruce [Picea jezoensis (Sieb. et Zucc.) Carr, var. jezoensis]

Table 1. Composition of kenaf samples Parameter VN kenaf VN kenaf CH kenaf CH kenaf Spruce Beech bast ﬁber fabric bast ﬁber core

Ash 8.6 2.0 16.7 9.6 2.8 5.0 Calcium 1.5 1.3 1.4 2.7 1.3 1.0 Magnesium 0.4 0.5 0.4 1.0 0.1 0.5 Lignin 111 117 130 200 327 258 Neutral sugars Fucose 1 0 0 0 0 0 Rhamnose 4 4 3 0 0 4 Arabinose 3 3 4 0 12 5 Xylose 171 158 162 195 81 216 Mannose 10 8 19 6 146 29 Galactose 8 6 11 2 38 14 Glucose 344 348 345 308 283 261 Total 541 528 544 511 560 529 Uronic acid 45 56 52 63 12 47 Nitrobenzene oxidation Total yield 528 505 513 483 235 382 S/V ratio 6.97 7.02 7.48 4.20 0.0 2.12 Results are given as grams per kilogram of oven-dried matter VN kenaf bast fiber, bast fiber of variety VN-1 cultivated at Thu Duc district, Ho Chi Minh City,Vietnam; VN kenaf fabric, purified VN kenaf bast fiber; CH kenaf bast fiber and CH kenaf core, bast fiber and core of variety Chinpi-3 cultivated in China, respectively; Spruce, Picea jezoensis (Sieb. Et Zucc.) Carr, var. jezoensis; Beech, Fagus crenata Blume; S/V, molar ratio of syringyl nuclei to guaiacyl nuclei 257 and beech (Fagus crenata Blume). Bast fiber was character- It has been reported that lignin of kenaf bast fiber ized by a significantly low lignin content and a high glucose is characterized by an unusually high SV molar ratio (7 to content (i.e., cellulose content). These results were similar 9).14,17–20 It would be interesting to make clear how lignin to those reported by Neto et al.55 for neutral sugar compo- with a high S/V ratio is deposited during maturation of the sition and by Pappas et al.18 for lignin content determined plant. A significantly high S/V ratio was observed in bast by near-infrared (NIR) spectroscopy. The structural fea- fiber lignin even in young plants (36 days after sowing), but tures of bast fiber lignin were characterized by a high total it leveled off at 50 days after sowing, whereas the levels of yield of alkaline nitrobenzene oxidation products and a core and root lignins remained low. The total yield of markedly high syringyl/guaiacyl nuclei molar ratio (S/V ra- alkaline nitrobenzene oxidation products increased with tio). Abbott et al.56 reported the S/V ratio of the kenaf bast fiber to be 2.0, whereas Ralph17 reported a significantly high S/V ratio of kenaf bast fiber lignin (7 to 9), similar to the results of this study. The high total yield of alkaline nitrobenzene oxidation products of bast fiber lignin suggests less condensed intermonomer linkages. The calcium content in kenaf samples, which may be related to the presence of pectin, was not significantly different from those of spruce and beech. Biomass accumulated in proportion to the exponential increase in days after sowing during maturation of the plants (Fig. 1), reaching 100g/plant (oven-dried weight) and 200–230cm height at 121 days after sowing. These results are similar to the results of Ahmad et al.57 The relative contents of lignin and cellulose increased, on the other hand, both 80% EtOH and H2O extracts de- creased during maturation of kenaf plants for all fractions of the tissues (Tables 2, 3). There were no significant differences in the major chemical composition between cores and roots for both Chinpi-3 and Everglades (data not shown for Everglades). The lignin content of bast fiber was about half that of the cores of roots, and the same level as in the matured samples described above for elder plants more than 50 days after sowing (Table 1). Morrison et al.58 reported a low content of ester- and ether-linked hydroxycinnamic acids (p-coumaric acid and ferulic acid) at the bottom core of kenaf plants harvested 96 and 151 days after sowing. However, hydroxycinnamic acids comprised less than 0.1% of the extract-free samples in this study (data not shown) probably because of significantly immature samples compared with those reported by Morrison et al.58 The acetyl content was almost constant throughout the extract- free samples: 2.2% for bast fiber and 1.5% for stem core and Fig. 1. Growth of kenaf varieties (Everglades and Chinpi-3), measured root. by dry weight

Table 2. Changes in extractives during maturing of kenaf plant (Chinpi-3) Days Bast ﬁber Core Root

80% EtOH H2O Total 80% EtOH H2O Total 80% EtOH H2O Total

30 160 100 259 160 100 259 158 105 363 36 187 80 267 217 87 304 191 53 244 44 170 96 266 213 100 315 131 52 183 49 143 83 226 218 106 316 151 54 205 52 135 65 200 181 79 260 107 58 165 59 135 80 215 174 89 263 121 64 185 68 115 72 187 158 82 240 122 52 174 90 98 75 173 128 78 206 98 44 142 121 103 50 153 132 38 170 117 27 144 Results are given as grams per kilogram of oven-dried sample 258

Table 3. Changes in neutral sugar composition, uronic acid, and lignin content of kenaf (Hibiscus cannabinus L. var Chinpi-3) during maturation Days after Change in neutral sugars Change in Change in sowing uronic acid lignin Rha Ara Xyl Man Gal Glc Total

Core 36 10 (1.5) 26 (1.2) 122 (9.3) 22 (1.7) 36 (3.1) 521 (15.1) 738 (13.1) 83 (4.2) 93 (3.5) 49 9 (1.5) 24 (1.7) 141 (7.0) 19 (2.1) 28 (3.6) 580 (10.7) 801 (7.6) 60 (6.1) 110 (6.4) 59 10 (1.2) 25 (1.5) 139 (3.5) 19 (2.9) 23 (4.0) 598 (9.0) 813 (6.4) 62 (4.5) 121 (7.0) 90 8 (1.2) 24 (2.3) 131 (6.4) 16 (1.2) 28 (4.5) 597 (10.6) 804 (15.4) 71 (3.1) 124 (1.5) 121 10 (2.1) 22 (1.5) 135 (5.6) 22 (3.1) 21 (2.5) 591 (12.1) 801 (7.6) 69 (4.2) 132 (7.2) Bast ﬁber 36 10 (2.1) 14 (2.0) 205 (8.9) 20 (1.2) 32 (3.2) 442 (6.1) 723 (9.8) 52 (5.5) 183 (3.5) 49 10 (4.4) 13 (1.1) 208 (6.5) 18 (1.7) 28 (3.5) 449 (5.9) 726 (11.2) 57 (5.5) 203 (4.6) 59 9 (2.6) 13 (1.5) 211 (3.0) 17 (1.7) 22 (1.5) 448 (3.5) 721 (5.0) 44 (2.6) 232 (4.5) 90 9 (1.1) 11 (1.5) 208 (6.6) 19 (1.5) 17 (1.7) 452 (6.8) 716 (3.8) 46 (3.6) 230 (6.7) 121 10 (1.1) 9 (1.5) 210 (6.6) 17 (1.5) 16 (1.7) 461 (6.8) 723 (3.8) 42 (3.6) 232 (6.7) Root 36 8 (2.0) 18 (2.5) 199 (11.7) 13 (1.0) 23 (2.1) 411 (9.5) 672 (3.5) 62 (3.6) 192 (3.0) 49 8 (1.0) 21 (2.0) 198 (4.6) 10 (1.5) 22 (1.5) 422 (8.0) 681 (13.5) 50 (4.6) 204 (2.6) 59 8 (1.0) 17 (2.1) 196 (5.2) 11 (1.0) 21 (1.5) 443 (9.3) 696 (16.6) 44 (2.0) 212 (6.1) 90 10 (1.5) 16 (0.6) 200 (6.4) 9 (2.1) 18 (1.7) 449 (6.1) 702 (5.9) 42 (4.9) 209 (3.8) 121 7 (2.6) 14 (1.5) 195 (2.0) 10 (1.5) 21 (1.5) 456 (5.5) 703 (4.2) 40 (5.9) 218 (6.4) Results are given grams per kilogram of extract-free sample: means of three samples and the SD (in parentheses)

Table 4. Changes in alkaline nitrobenzene oxidation products of kenaf (Hibiscus cannabinus var. Chinpi-3) during maturation Days after Bast ﬁber Core Root sowing Yield S/V Yield S/V Yield S/V

30 48 (4.6) 2.38 (0.070) – – 226 (4.2) 1.28 (0.082) 36 49 (2.5) 4.03 (0.056) 237 (8.5) 1.20 (0.091) 269 (7.0) 1.59 (0.069) 45 88 (5.0) 4.63 (0.053) 244 (3.5) 1.30 (0.067) 262 (4.0) 1.78 (0.054) 50 137 (3.1) 4.94 (0.074) 278 (7.5) 1.29 (0.048) 266 (4.6) 1.80 (0.088) 53 193 (3.8) 5.33 (0.092) 293 (6.6) 1.32 (0.040) 263 (4.2) 1.82 (0.074) 60 248 (3.5) 5.57 (0.087) 299 (5.5) 1.34 (0.055) 268 (3.0) 1.84 (0.061) 70 262 (1.5) 5.87 (0.053) 305 (4.0) 1.42 (0.060) 272 (7.0) 1.92 (0.048) 91 291 (7.1) 5.67 (0.075) 324 (5.0) 1.48 (0.040) 269 (8.4) 1.88 (0.060) 122 297 (6.1) 5.99 (0.096) 325 (9.3) 1.58 (0.079) 276 (5.8) 1.95 (0.082) There were three samples for each measurement reported Yield, total yield of alkaline nitrobenzene oxidation products (grams per kilogram of lignin determined by an acetyl bromide procedure); S/V, molar ratio of products with syringyl nuclei/products with guaiacyl nuclei

Table 5. Characterization of Björkman lignin prepared from maturing Table 6. Rate of photosynthesis of leaves of maturing kenaf (Hibiscus kenaf (Hibiscus cannabinus L. var. Chinpi-3) 121 days after sowing cannabinus var. Chinpi-3 and var. Everglades) and other plants Parameter Fiber Core Leaves Plant Latin name PN SD

Yield (g/kg of AcBr lignin) 422 389 154 Kenaf Acetyl group (g/kg of sample) 121 33 30 Chinpi-3 Hibiscus cannabinus var. Chinpi-3 23.4 2.99 Nitrobenzene oxidation Everglades Hibiscus cannabinus var. Everglades-3 22.6 1.97 Yield (g/kg)a 264 293 224 Konara Quercus serrata Thunb. 8.7 0.33 S/V ratio 5.78 1.44 1.78 Ubamegashi Quercus phillyraeoides A. Gray 7.3 1.24 a Ichijiku Ficus carica L. 7.0 1.00 Total yield of alkaline nitrobenzene oxidation products (g/kg of Sangojyu Viburnum awabuki K. Koch 6.2 0.92 sample) Ajisai Hydrangea macrophylla Seringe 5.2 0.42 Ichyou Ginkgo biloba L. 4.3 0.30 Nanakamado Sorbus commixta Hedlund 4.3 0.35 maturation of the kenaf plant (Table 4), but there were no Sudajii Shiia Sieboldii Makino 3.4 0.57 Kunugi Quercus acutissima Carruth 2.5 – signiﬁcant differences between the bast ﬁber, cores and µ 2 roots. PN, rate of photosynthesis ( mol CO2/m /s) at a photon density of 1000 µmol /cm2/s

Structural features of Björkman lignin of maturing kenaf Björkman’s procedure.54 The structure of the lignins was characterized by an alkaline nitrobenzene oxidation, acetyl Björkman lignins were isolated from bast ﬁber, cores and group determination, and measurement of 1H-NMR spectra leaves of maturing kenaf (121 days after sowing) with the after acetylation with acetic anhydride/pyridine. The 13C- 259

Table 7. CO2 ﬁxation by plants

Plant C CO2 Biomass Accumulation (t/ha/y) (t/ha/y) (t/ha/y) m3/ha Speciﬁc gravity Tons % Increase

Japanese treea Takayama 0.67 2.5 1.4 120 0.4 48 3.5 Kiyosumi 1.36 5.0 2.7 120 0.4 48 7.1 Tropical rain forestb 4.5 16.5 9.0 180 0.7 126 8.9 Melaleuca cajuputi c Dry acidic swamp 5.7 20.9 11.4 180 0.8 144 9.9 Wet acidic swamp 10 36.7 20.0 180 0.8 144 17.4 Philippines treed Mahogany 3.8 13.8 7.5 180 0.6 108 6.9 Narra 5.0 18.3 10.0 180 0.6 108 9.3 Kenafe 18–37 66–135 37–75 Cultivation density: 220,000 – 500,000 plants/ha t/ha/y, tons per hectare per year a Cryptomeria japonica D. Don. Determined by Tange et al.59 at Takayama and Kiyosumi b Dipterocarpaceae spp. Determined by Tange et al.59 in Malaysia c Determined by Yamanoshita et al.60 in dry and wet acidic swamps d Determined by Iiyama et al. at Los Banos, Philippines for mahogany (Swietenia macrophylla King) and narra (Pterocarpus indicus Willd.) e Determined by L.Q. Hung in Thu Duc District, Ho Chi Minh City, Vietnam

Fig. 2. 1H nuclear magnetic resonance (1H-NMR) spectra of acetylated Björkman lignin isolated from bast ﬁber (a), core (b), and leaves (c) of variety Chinpi-3 of the kenaf plant (121 days after sowing) 260 a rected for photon density and calculated to be 1000µmol/ cm2/s. Kenaf plants showed an extremely high rate of photosynthesis, about 3–10 times higher than those of temperate plants (Table 6).

Fixation of CO2 is a function not only of the photosynthesis rate of plants but also of their cultivation density. Kenaf (Hibiscus cannabinus L. var. VN-1) was cultivated under various densities (222000–555000 plants/ha) at Thu Duc District, Ho Chi Minh City, Vietnam. The growth of the plants was not affected by the cultivation density (Fig. 3), and the biomass accumulated was 100g/plant (dry weight), with a standard deviation of 8.3g, which corre-

sponds to the net ﬁxation of 183g CO2/plant. The CO2 ﬁxation by kenaf was compared with that of trees grown under different conditions (Table 7).

Acknowledgments This project was supported by the Science and Technology Agency (STA) fellowship of the Japan International Sci- ence and Technology Exchange Center (JISTEC), which has been successfully applied by Dr. Shuji Hosoya, Forestry and Forest Products Research Institute. We thank Dr. Toshio Sumizono and Mr. Masao b Sakurai, Forestry and Forest Products Research Institute, for their kind help in determining the rate of photosynthesis and cultivating the kenaf plants, respectively. We also express our appreciation to Dr. Quang Hung Le, College of Agriculture and Forestry, Ho Chi Minh City, Vietnam for offering information about the cultivation of kenaf at Thu Duc District, Ho Chi Minh City.

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